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Current IssueEditorial BoardOnline First ArticlesArchive

Review Article

Red Beetroot (Beta vulgaris L. var rubra L.) is a Potential Source of Nitrate as a Functional Food: A Review

T
T.D. Widyaningsih1
A
A.H. Fitriah1,*
S
S.N. Wulan1
H
H. Sujuti2
1Department of Food Science and Biotechnology, Brawijaya University, Jl. Veteran No. 10-11, Ketawanggede, Lowokwaru District, Malang City, East Java 65145, Indonesia.
2Faculty of Medicine, Brawijaya University, Jl. Veteran No. 10-11, Ketawanggede, Lowokwaru District, Malang City, East Java 65145, Indonesia.

ABSTRACT

Beetroot is known for the common varieties which are the red beetroot (Beta vulgaris L.var Rubra L.), characterized by a dark red  tuber and the white beetroot/cut beetroot (Beta vulgaris  L. var  Cicla  L.) with a whitish red tuber. Beetroot is also known for its potential bioactive content, such as nitrate, phenolics, betalains, ascorbic acid, carotenoids and saponins, which are processed into various functional foods of high nutritional value. This article aims to review role of the nitrate as a bioactive compound in red beetroot, its benefits as a functional food ingredient and its benefits for health. The research was conducted at Brawijaya University Malang, Indonesia during 2024. Nitrate is a major potential component in beetroot that  has  been  widely  studied  as  an implementation  in  health  improvement  such  as  metabolic disorders. Nitrate is naturally formed in plants and subsequently converted to nitric oxide (NO) in the human body which is known to have beneficial effects for clinical application. NO could regulate  metabolic disorder-induced metabolic diseases, such as reduced blood pressure, increased oxygen, nutrient delivery to the active muscle and mediator for neurotransmission, vasodilatation, nerve function and also as immune defense. Beetroot can have added value if it is converted into a functional product. Beetroot can be formulated as a fresh product, fermented, bread, powder, chips, gel and cereal bar. Functional beetroot production can be a new strategy for increasing the nutritional content with high bioaccessibility such as nitrate, potassium and antioxidants which have the potential to improve heart health and sports performance.

INTRODUCTION

Beetroots are plants that have been grown for medicinal purposes for thousands of years. According to records written in Europe, beetroots were cultivated before the tenth century (Yashwant 2015). Beetroots are a type of root vegetable source of natural antioxidants (Chhikara et al., 2019),  a source of dietary fiber, a source of minerals (potassium, sodium, iron, copper, magnesium, calcium, phosphorus and zinc), a source of vitamins (retinol, ascorbic acid and B-complex), as well as being rich in bioactive compounds such as nitrate, carotenoids, ascorbic acids, triterpenes, betalains, phenolics and saponins mentioned in Fig 1 (Baião et al., 2016; Chhikara et al., 2019; Clifford et al., 2015; Hadipour et al., 2020) and often known as NO Diet (Baião et al., 2017; Nowacka et al., 2019) because it is rich in nitrate, so beetroot is a high-nitrate plant (Lidder and Webb, 2013). Dietary nitrates and nitrites serve as effective NO (Nitric Oxide) donors under conditions of hypoxia and ischemia (Bryan and Ivy, 2015). NO causes a vasodilatory effect and increases blood flow to the muscles (Moazami et al., 2015). It takes > 6.3 mmol to increase NO levels and decrease blood pressure in normal people and Cardio Vascular Disease (CVD) patients (Baião et al., 2020). The high nitrate content in beetroot juice can increase the athlete’s VO2 Max which biologically affects the utilization of O2 regulators by muscle contractors so that the distribution of O2 according to muscle needs and nitrate supplementation until the fifteenth day can increase mitochondrial mass so that it also increases the use of NO in mitochondria to produce energy (Sanrebayu et al., 2020).

Fig 1: Bioactive compounds in beets (Baião et al., 2016; Chhikara et al., 2019; Clifford et al., 2015; Hadipour et al., 2020).


       
Beetroots Originated in Mesopotamia and from Europe and Asia Minor in the 8th century. Several varieties of beet such as yellow beet (1700s) and sugar beet developed by the Prussians in the 1800’s, now the more popular red beetroot comes from the Mediterranean region, widely cultivated in Europe, America and throughout Asia (Chawla et al., 2016; Zohary et al., 2012). Two well-known beetroot varieties are the red beetroot (Beta vulgaris L. var Rubra L.) which is characterized by a dark red tuber and the white beetroot/cut beetroot (Beta vulgaris L.var cicla L.) with a whitish red tuber. Beetroots are a promising commodity for cultivation because they can be harvested every 2.5-3 months after the seeds are sown, Even though the two types of beetroots cannot flower and set seeds in Indonesia the seeds are still imported from abroad but can grow well in Indonesia, especially in the highlands with an altitude of > 1,000 m asl for red beetroots and at an altitude of 500 m asl for white beetroots. Beetroots are unable to form tubers if grown in lowlands. Therefore beetroots are widely grown on the island of Java, especially Cipanas, Lembang, Pangalengan and Batu (Asian Journal, 2017).     
       
At the stage of growth, beet plants need direct exposure to sunlight for around 6-8 hours. It needs regular watering especially when the topsoil is dry. It needs to be kept moist but not wet to avoid rot and fungus caused by excessive watering. The sowing season in Bangalore (India) is in July and August which is the best season for sowing seeds. The sowing method uses row sowing. Sow the seeds at a depth of 2 cm and each seed should be sown at intervals of 5-10 cm (GreenMyLife, 2018). Beetroots develop better in deep, looser, acidic soil that is rich in organic matter and light, the optimum temperature ranges from 10oC-20oC. The best color, taste and quality are achieved in cool weather through the stages of the reproductive cycle. The appearance of oval to heart-shaped leaves occurs in the vegetative phase, around the stem, which grows upright. Emission of flower tassels occurs with the production of 2-3 mm lenticular seeds, consisting of gromeruli during the reproductive stage. The root system consists of a main root and smaller roots with lateral branches. The taproot is dark purplish red, round to long in shape and develops almost at ground level (Kumar, 2015).
       
The way to benefit from beetroot, in the form of traditional formulas such as cooked vegetables or fresh juices, requires a very large amount of beetroot (Baião et al., 2016; 2017; 2018; Da Silva et al., 2016) but if too much will cause discomfort to the stomach and can cause nausea and vomiting. Beetroot juice is a source of nutrients and rich in bioactive compounds. Freshly extracted beetroot juice contains 62.20% Antioxidant activity, contains 990.7 mg/100 ml total phenols, 790 mg/L anthocyanins and 520.3 mg/L betanin, so it can be used as added value in food formulation (Arora et al., 2019). Therefore it is necessary to supplement beetroot with the right formulation and the appropriate portion as well as effective nitrate concentration and other bioactive compounds as an alternative that is suitable for consumption such as consuming natural vegetables, by maintaining the composition of nitrate and other bioactive compounds contained in beetroot (Baião et al., 2017).
       
This article aims to review nitrate as a bioactive compound in red beetroot, its benefits as a food ingredient, its mechanism as a functional food and its benefits for health.
 
Beta vulgaris
 
Beta vulgaris is also known as beetroot. Beetroots belong to the Chenopodiaceae family which includes around 1400 species which are divided into 105 genera (Chawla et al., 2016) and are members of the dicot family. Beetroots are classified in the Amarantaceae family, Genus Beta and Beta vulgaris species (Indonesian Ministry of Health, 2018). The edible part of the beetroot is the root. The main root is long, sharp and sturdy and the side roots form a dense texture. Roots are generally spherical or cylindrical in color red-purple/yellow-golden/red-white depending on the beetroot variety. Beetroot leaves emerge from the hypocotyl corolla and vary in leaf size, shape and color. Seeds are known as multigerm seeds because 1 seed can produce more than 1 sprout. The outer part of the cork seed contains phenolic compounds and inhibits germination as a physical barrier. The stems are decumbent, erect and branched a lot. The flowers are very small with 5 petals (Kezi and Sumathy, 2014). Here’s a description of beetroot’s different parts (Fig 2).

Fig 2: (A) Beet physiology, (B) Red beet physiology Biancardi, et al., 2010.


 
Taproot
 
This is the most commonly consumed part of the beetroot. It is a thick, fleshy taproot that can range in shape from globular to long and tapered. The skin is thin and smooth and while most people are familiar with the dark purplish-red variety, some beets can also be nearly white, orange, or even have concentric red and white rings. The flesh has a sweet and earthy taste and is often used in salads, soups, or as a side dish. 
 
Leaves (Beet greens)
 
The leaves that grow from the top of the taproot are also edible and nutritious. They are typically a dark green color with red petioles (leaf stems) and midribs. Beet greens can be cooked like spinach or chard and are rich in vitamins and minerals. 
 
Stems
 
The stems connecting the leaves to the root are also edible. They are often sautéed or used in stir-fries. 
       
All parts of the beetroot plant-the root, leaves and stems-are safe to eat and can be incorporated into a variety of dishes (Biancardi et al., 2010).
       
In order for beet plants to grow optimally to produce quality crops, it is necessary to control pests that can cause crop failure. Pest control can be done as follows:
1.  Flea beetles: do not threaten plants, only reduce value due to hollow leaves.
2.  Cercospora leaf spot disease: causes significant losses, especially in late summer (high temperature, high humidity, long leaf wet periods throughout the night). Impact: beets fail to grow to full size if severe. Controlled by spraying Mencozeb 2 g/L.
3.  Rhizoctonia Root Rot. Impact: kills and stunts plants. Controlled with Carbendazim 1 g/L (GreenMyLife, 2018).
 
The nutritional composition of beets in 100 grams of ingredients as stated in the 2017 Indonesian Food Comp-osition Table (TKPI) and 2018 United States Department  of Agriculture (USDA) can be seen in the Table 1.

Table 1: Composition of nutrients in 100 g of beets.


     
Beets not only consist of macronutrients and micronutrients, but beets are a functional food source because they have benefits for various diseases by containing important components called bioactive compounds such as vitamins, minerals, phenols, carotenoids, nitrates, ascorbic acid and betalains. The effects of phytochemicals depend on the bioaccessibility of nutrients during the digestive process (Liliana and Oana-Viorela, 2020).
       
Beets are also a plant that is rich in nitrates, so beets are a plant that is high in nitrate content. Table 2 shows the average nitrate content in vegetables in mg/kg, mmol in UK portions as a guide to estimating the number of nitrate units per portion (1 nitrate unit = 1 mmol) to estimate nitrate intake or to modify/alter intake as desired. Tap water and mineral water are included in the table intended for comparison (Lidder and Webb, 2013).

Table 2: Nitrate content in plants (Lidder dan Webb 2013).


       
Beetroot are an important source of inorganic nitrate with varying amounts of nitrate. It is reported that there is a 10-fold variation between single varieties (Mirmiran, 2020). Some studies report nitrate levels in beetroot ranging from 644 - 1800 mg/kg (Lidder and Webb, 2013), although some studies found higher amounts of nitrate in beetroot, such as beetroot juice containing 4965 mg/L nitrate (Corleto et al., 2018). Raw beetroot contains 4420 mg/kg but this amount increases drastically to 42415 mg/kg after the dehydration process (Sucu and Turp, 2018), likewise, beetroot powder contains 14037 mg/kg nitrate (Ozaki et al., 2021). In addition, fermenting beetroot juice and extract allows the conversion of nitrates to nitrites first (Choi et al., 2017), thus increasing the protective effect, which can be added to meat products in the form of nitrites (Hwang et al., 2017; 2018).
 
Nitrate and nitrite production in plants
 
Nitrate  and  nitrite  is  produced  in  plant  by  nitrogen  cycle.  Nitrogen  cycle  is  a fundamental biogeochemical process of a crop development that converts nitrogen into various forms,  allowing  it  to  move  from  the  atmosphere  to  the  soil,  organisms,  and  back  to  the atmosphere (Astier; 2018; Valenzuela, 2023). Atmospheric N becomes available to plants via a series of microbial transformations in the soil (Geisseler, 2010; Grzyb, 2021). The process of the  nitrogen  cycle  consists  of  several  stages,  including  nitrogen  fixation, nitrification, assimilation, ammonification and  denitrifi-cation  (Grzyb, 2021; Brochado et al., 2023).  Nitrogen fixation is the initial step of the nitrogen cycle, where atmospheric nitrogen (N2) is converted into ammonia (NH3).The symbiotic nitrogen fixation is an indispensable process in the nitrogen cycle, where bacteria of the genus Rhizobium establish symbiotic associations with leguminous plants, such as the common bean (Phaseolus vulgaris), soybean (Glycine max) and pea (Pisum sativum) (Brito, 2011; Cunha, 2023; Kamran, 2023). These bacteria have the ability to convert atmospheric nitrogen into a form assimilable by plants (Brochado et al., 2023).
       
After nitrogen fixation, the next stages is nitrification which converting ammonia (NH3) into nitrite (NO2) and then into nitrate (NO3). This process is carried out by nitrifying bacteria in the soil, ammonia (NH3) is first converted into nitrite by Nitrosomonas bacteria and then into nitrate by Nitrobacter bacteria. Nitrates (NO3) are the primary source of nitrogen for plants and they  can  be  taken  up  by  plant  roots and used  to  synthesize  amino  acids  and other nitrogen- containing compounds (Valenzuela, 2023). Nitrification plays a crucial role in transforming organic nitrogen compounds into readily accessible inorganic forms for plants  (Brochado, 2023).
       
Assimilation is a next stages that incorporating ammonia (NH3) and nitrates (NO3-) into biological tissues, such as plant and animal cells. This incorporation allows organisms to utilize nitrogen for the synthesis of essential molecules, such as proteins and nucleic acids (Mokhele, 2012,  Zhu, 2023).  After  assimilation,  processing  of  ammonification  occur  when  organisms excrete  waste  or  die, the  nitrogen  in  their  tissues  is  in  the  form  of  organic  nitrogen.  Various fungi and prokaryotes then decompose the tissue and release inorganic nitrogen back into the environment,  making it available for uptake by plants and other  microorganisms for growth (Kuypers, 2018). Nitrate-N that is not taken up by plants, because it is soluble, may be leached below  the root  zone, it may be converted to  dinitrogen (N2) or nitrous  oxide  (N2O)  gases  by heterotrophic bacteria, called denitrification process (Grzyb, 2021; Wang, 2022).
 
Red beetroot as a functional food
 
Benefits of red beetroot as a functional ingredient in various food products
 
Beetroots can have added value if they can be made into a product (Table 3). Beetroot can be formulated as fresh juice, fermented juice, bread, powder, chips, gel and cereal-bar which have been tested on healthy and unhealthy volunteers as a food supplement. Several products made from red beetroot are in great demand among the public, such as juice, yogurt, candy, jam, jelly, powder and ice cream (Czyżewska et al., 2006; Baião et al., 2017; 2018; Hobbs et al., 2014). Red beetroot is a tuber vegetable rich in nutrients and bioactive compounds, traditionally used in various food products because of its red color. Cereal-based products such as bread, pastries, biscuits, pasta and noodles are food sources of carbohydrates and protein but lack micronutrients and fiber, thereby increasing consumer demand for healthy foods that provide nutrient-dense foods (Rousta et al., 2021).

Table 3: Application of red beetroot in food products (Sneh et al. 2022).


       
The addition of red beetroot fiber to bread, rolls, cakes, cupcakes, biscuits and cookies can increase the fiber, ash and protein content while reducing the fat content due to the higher nutritional content of beetroot powder (Hobbs et al., 2014; Nagib and Zidan 2019;  Daunaravičiūtė et al., 2020). Beetroots can be added to ready-to-eat snacks such as extruded products and breakfast cereals. Formulated as a functional snack with an attractive pink to red color it is very popular with consumers because of its delicious taste, texture and attractive appearance (Abdul Alam et al., 2018; Lisiecka and Wójtowicz, 2021). Red beetroot powder and beetroot juice can be used as a natural coloring in butter, mayonnaise, cream cheese spread and cream cheese which functions as a natural antimicrobial, reduces lipid oxides, suppresses the growth of bacteria and fungi and reduces peroxide levels. This is because the antioxidant activity of beetroots is higher, resulting in dairy products with a longer shelf life (Raikos et al., 2016, Asadaii et al., 2020).
       
The addition of beetroots in milk-based drinks such as yogurt and fermented buttermilk drinks can reduce acidity, increase antioxidant properties, antibacterial potential, total phenolic content, survival of probiotic bacteria Streptococcus thermophiles and Lactobacillus and increase consumer acceptance (Ganguly et al., 2017; Hashem 2018; Ahmad and Ali, 2019). The addition of 10% red beetroot powder to cookies is more acceptable (Murlidhar et al., 2017) and the quality of spray-dried beetroot powder stored for a long period is better stored in LAP packaging compared to HDPE (Singh and Hathan, 2017). The addition of 10% beetroot powder can also increase the elasticity of snack bars, significantly reduce hardness, the most acceptable texture and sensory properties, have higher ash content, carbohydrates, antioxidant activity, flavonoids and total phenols (Tangariya et al., 2022). Consumption of functional beetroot gelly is a new strategy to provide nutritional content with high bioaccessibility such as nitrate, potassium and antioxidants which have the potential to improve heart health and sports performance (Silva et al., 2016; Morgado et al., 2016).
 
Health benefits of nitrate and nitrite in red beetroot
 
Nitrates (NO3-)  and  nitrites  (NO2-)  are  naturally  occurring  substances  in  fruits  and   vegetables, which humans are encouraged to consume because of their beneficial health effects. On the other side, nitrates and nitrites are used as food additives such as sausages, ham and other processed meat (Levine, 2012; Song, 2015). Nitrate and nitrite in humans are present due to diet or produced by the action of endogenous L-arginine-NO synthase (Nuji, 2017; Mcneal, 2021). Nitrate (NO3-) in food is converted in the human body to nitrite (NO2-) and subsequently to nitric oxide (NO) generated by NOS (NO synthase) enzymes that oxidize in the blood and tissue. In the blood, exogenous NO3 mixes with endogenous NO3- produced via the oxidation of NO (Shannon, 2021; Redaelli, 2022).
       
Nitric oxide in the body is a compound that is known to have beneficial effects for clinical application. NO could regulate metabolic disorder-induced cardiovascular diseases and other metabolic disease, such as reduced blood pressure and increased oxygen and nutrient delivery to the active muscle and also as a mediator for neurotrans-mission, vasodilatation, nerve function and immune defense (Ma, 2018; Zamani, 2021; Andrabi, 2023). Under conditions of illness or senescence, the activity of eNOS (endothelial nitric oxide synthase) was reduced  and  the production of NO was decreased  (Novensa, 2011; Rogers, 2013). Thus indicating exogenous source of NO supplement might have a potential treatment for patients undergoing illness or senescence (Ma, 2018).
       
NO is known to be a potent vasodilator to cause a BP reduction. NO generated in the vasculature causes  relaxation in vascular smooth  muscle,  which  subsequently  results in vasodilation (Levine, 2012; Redaelli, 2022). The nitrite anion is a cell-signaling molecule, which is considered a storage pool of NO as well as a NO-independent signal. Dietary nitrate- enhanced nitrite is capable of increasing cyclic guanosine 32 ,52 -monophosphate (cGMP) levels in tissues and contributing to blood vessel vasodilation via a mechanism that lies upstream from activation of soluble guanylyl cyclase (sGC) (Liu, 2020).
       
Moreover, the synthesis of NO was reduced in obese mice (Siervo, 2011). Metabolic disorder-induced high blood pressure, insulin resistance and carbohydrate tolerance were found in eNOS (endothelial nitric oxide synthase)-knockout mice. Dietary nitrate effectively supplements NO by the activated exogenous NO3-NO2-NO pathway under conditions of hypoxia. Nitrate enhanced exercise tolerance by the NO-cGMP-PPAR pathway and increased the metabolism of fatty acid in skeletal muscle cells (Ashmore, 2015). Exogenous nitrate could activate the cGMP pathway in mice and promote the conversion of white adipose to brown adipose, therefore enhancing fat metabolism and decreasing body weight (Roberts, 2015).
               
NO also contributes to improved wound healing by upregulating angiogenic factors, such as TGF-ß and VEGF, which ensures adequate blood supply for healing. However, in cases of impaired wound healing, inadequate NO synthases and low levels of available NO lead to decreased collagen deposition, unregulated inflammatory responses, tissue hypoxia and prolonged healing time (Malone-Povolny, 2019). Recently, hypoxia-induced oxidative stress conditions have been suggested to facilitate the depletion of antioxidants and thus promote cysteine oxidation and subsequently lead to an enhanced Cgb generation of NO in the presence of nitrite during hypoxia (Bescós, 2012; Reeder, 2018).

CONCLUSION

Red beetroot is a superfood that has been used as a therapeutic and functional food ingredient since ancient times. This paper summarizes the entire scope of red beetroot and its use as a value-added product. It is useful as a food coloring agent in many dairy and food products. The Nitrate content in red beets through the physiological role of NO which functions as vasodilation, efficient use of O2 during exercise, the immune system, as a neurotransmitter and as an inhibitor of platelet adhesion. It also has anti-microbial, anti-hypertensive, anti- inflammatory, anti-hyperglycemic properties, etc. This plant has many health benefits and provides an opportunity for researchers to develop various products derived from red beets that have added value.

ACKNOWLEDGEMENT

The present study was supported by Brawijaya University and the Ministry of Health of the Republic of Indonesia through the Malang Ministry of Health Health Polytechnic.
 
Disclaimers
 
The views and conclusions expressed in this article are solely those of the authors and do not necessarily represent the views of their affiliated institutions. The authors are responsible for the accuracy and completeness of the information provided, but do not accept any liability for any direct or indirect losses resulting from the use of this content.

Informed consent
 
All animal procedures for experiments were approved by the Committee of Experimental Animal care and handling techniques were approved by the University of Animal Care Committee.

CONFLICT OF INTEREST

The authors declare that there are no conflicts of interest regarding the publication of this article. No funding or sponsorship influenced the design of the study, data collection, analysis, decision to publish, or preparation of the manuscript.

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    Review Article

    Red Beetroot (Beta vulgaris L. var rubra L.) is a Potential Source of Nitrate as a Functional Food: A Review

    T
    T.D. Widyaningsih1
    A
    A.H. Fitriah1,*
    S
    S.N. Wulan1
    H
    H. Sujuti2
    1Department of Food Science and Biotechnology, Brawijaya University, Jl. Veteran No. 10-11, Ketawanggede, Lowokwaru District, Malang City, East Java 65145, Indonesia.
    2Faculty of Medicine, Brawijaya University, Jl. Veteran No. 10-11, Ketawanggede, Lowokwaru District, Malang City, East Java 65145, Indonesia.

    ABSTRACT

    Beetroot is known for the common varieties which are the red beetroot (Beta vulgaris L.var Rubra L.), characterized by a dark red  tuber and the white beetroot/cut beetroot (Beta vulgaris  L. var  Cicla  L.) with a whitish red tuber. Beetroot is also known for its potential bioactive content, such as nitrate, phenolics, betalains, ascorbic acid, carotenoids and saponins, which are processed into various functional foods of high nutritional value. This article aims to review role of the nitrate as a bioactive compound in red beetroot, its benefits as a functional food ingredient and its benefits for health. The research was conducted at Brawijaya University Malang, Indonesia during 2024. Nitrate is a major potential component in beetroot that  has  been  widely  studied  as  an implementation  in  health  improvement  such  as  metabolic disorders. Nitrate is naturally formed in plants and subsequently converted to nitric oxide (NO) in the human body which is known to have beneficial effects for clinical application. NO could regulate  metabolic disorder-induced metabolic diseases, such as reduced blood pressure, increased oxygen, nutrient delivery to the active muscle and mediator for neurotransmission, vasodilatation, nerve function and also as immune defense. Beetroot can have added value if it is converted into a functional product. Beetroot can be formulated as a fresh product, fermented, bread, powder, chips, gel and cereal bar. Functional beetroot production can be a new strategy for increasing the nutritional content with high bioaccessibility such as nitrate, potassium and antioxidants which have the potential to improve heart health and sports performance.

    INTRODUCTION

    Beetroots are plants that have been grown for medicinal purposes for thousands of years. According to records written in Europe, beetroots were cultivated before the tenth century (Yashwant 2015). Beetroots are a type of root vegetable source of natural antioxidants (Chhikara et al., 2019),  a source of dietary fiber, a source of minerals (potassium, sodium, iron, copper, magnesium, calcium, phosphorus and zinc), a source of vitamins (retinol, ascorbic acid and B-complex), as well as being rich in bioactive compounds such as nitrate, carotenoids, ascorbic acids, triterpenes, betalains, phenolics and saponins mentioned in Fig 1 (Baião et al., 2016; Chhikara et al., 2019; Clifford et al., 2015; Hadipour et al., 2020) and often known as NO Diet (Baião et al., 2017; Nowacka et al., 2019) because it is rich in nitrate, so beetroot is a high-nitrate plant (Lidder and Webb, 2013). Dietary nitrates and nitrites serve as effective NO (Nitric Oxide) donors under conditions of hypoxia and ischemia (Bryan and Ivy, 2015). NO causes a vasodilatory effect and increases blood flow to the muscles (Moazami et al., 2015). It takes > 6.3 mmol to increase NO levels and decrease blood pressure in normal people and Cardio Vascular Disease (CVD) patients (Baião et al., 2020). The high nitrate content in beetroot juice can increase the athlete’s VO2 Max which biologically affects the utilization of O2 regulators by muscle contractors so that the distribution of O2 according to muscle needs and nitrate supplementation until the fifteenth day can increase mitochondrial mass so that it also increases the use of NO in mitochondria to produce energy (Sanrebayu et al., 2020).

    Fig 1: Bioactive compounds in beets (Baião et al., 2016; Chhikara et al., 2019; Clifford et al., 2015; Hadipour et al., 2020).


           
    Beetroots Originated in Mesopotamia and from Europe and Asia Minor in the 8th century. Several varieties of beet such as yellow beet (1700s) and sugar beet developed by the Prussians in the 1800’s, now the more popular red beetroot comes from the Mediterranean region, widely cultivated in Europe, America and throughout Asia (Chawla et al., 2016; Zohary et al., 2012). Two well-known beetroot varieties are the red beetroot (Beta vulgaris L. var Rubra L.) which is characterized by a dark red tuber and the white beetroot/cut beetroot (Beta vulgaris L.var cicla L.) with a whitish red tuber. Beetroots are a promising commodity for cultivation because they can be harvested every 2.5-3 months after the seeds are sown, Even though the two types of beetroots cannot flower and set seeds in Indonesia the seeds are still imported from abroad but can grow well in Indonesia, especially in the highlands with an altitude of > 1,000 m asl for red beetroots and at an altitude of 500 m asl for white beetroots. Beetroots are unable to form tubers if grown in lowlands. Therefore beetroots are widely grown on the island of Java, especially Cipanas, Lembang, Pangalengan and Batu (Asian Journal, 2017).     
           
    At the stage of growth, beet plants need direct exposure to sunlight for around 6-8 hours. It needs regular watering especially when the topsoil is dry. It needs to be kept moist but not wet to avoid rot and fungus caused by excessive watering. The sowing season in Bangalore (India) is in July and August which is the best season for sowing seeds. The sowing method uses row sowing. Sow the seeds at a depth of 2 cm and each seed should be sown at intervals of 5-10 cm (GreenMyLife, 2018). Beetroots develop better in deep, looser, acidic soil that is rich in organic matter and light, the optimum temperature ranges from 10oC-20oC. The best color, taste and quality are achieved in cool weather through the stages of the reproductive cycle. The appearance of oval to heart-shaped leaves occurs in the vegetative phase, around the stem, which grows upright. Emission of flower tassels occurs with the production of 2-3 mm lenticular seeds, consisting of gromeruli during the reproductive stage. The root system consists of a main root and smaller roots with lateral branches. The taproot is dark purplish red, round to long in shape and develops almost at ground level (Kumar, 2015).
           
    The way to benefit from beetroot, in the form of traditional formulas such as cooked vegetables or fresh juices, requires a very large amount of beetroot (Baião et al., 2016; 2017; 2018; Da Silva et al., 2016) but if too much will cause discomfort to the stomach and can cause nausea and vomiting. Beetroot juice is a source of nutrients and rich in bioactive compounds. Freshly extracted beetroot juice contains 62.20% Antioxidant activity, contains 990.7 mg/100 ml total phenols, 790 mg/L anthocyanins and 520.3 mg/L betanin, so it can be used as added value in food formulation (Arora et al., 2019). Therefore it is necessary to supplement beetroot with the right formulation and the appropriate portion as well as effective nitrate concentration and other bioactive compounds as an alternative that is suitable for consumption such as consuming natural vegetables, by maintaining the composition of nitrate and other bioactive compounds contained in beetroot (Baião et al., 2017).
           
    This article aims to review nitrate as a bioactive compound in red beetroot, its benefits as a food ingredient, its mechanism as a functional food and its benefits for health.
     
    Beta vulgaris
     
    Beta vulgaris is also known as beetroot. Beetroots belong to the Chenopodiaceae family which includes around 1400 species which are divided into 105 genera (Chawla et al., 2016) and are members of the dicot family. Beetroots are classified in the Amarantaceae family, Genus Beta and Beta vulgaris species (Indonesian Ministry of Health, 2018). The edible part of the beetroot is the root. The main root is long, sharp and sturdy and the side roots form a dense texture. Roots are generally spherical or cylindrical in color red-purple/yellow-golden/red-white depending on the beetroot variety. Beetroot leaves emerge from the hypocotyl corolla and vary in leaf size, shape and color. Seeds are known as multigerm seeds because 1 seed can produce more than 1 sprout. The outer part of the cork seed contains phenolic compounds and inhibits germination as a physical barrier. The stems are decumbent, erect and branched a lot. The flowers are very small with 5 petals (Kezi and Sumathy, 2014). Here’s a description of beetroot’s different parts (Fig 2).

    Fig 2: (A) Beet physiology, (B) Red beet physiology Biancardi, et al., 2010.


     
    Taproot
     
    This is the most commonly consumed part of the beetroot. It is a thick, fleshy taproot that can range in shape from globular to long and tapered. The skin is thin and smooth and while most people are familiar with the dark purplish-red variety, some beets can also be nearly white, orange, or even have concentric red and white rings. The flesh has a sweet and earthy taste and is often used in salads, soups, or as a side dish. 
     
    Leaves (Beet greens)
     
    The leaves that grow from the top of the taproot are also edible and nutritious. They are typically a dark green color with red petioles (leaf stems) and midribs. Beet greens can be cooked like spinach or chard and are rich in vitamins and minerals. 
     
    Stems
     
    The stems connecting the leaves to the root are also edible. They are often sautéed or used in stir-fries. 
           
    All parts of the beetroot plant-the root, leaves and stems-are safe to eat and can be incorporated into a variety of dishes (Biancardi et al., 2010).
           
    In order for beet plants to grow optimally to produce quality crops, it is necessary to control pests that can cause crop failure. Pest control can be done as follows:
    1.  Flea beetles: do not threaten plants, only reduce value due to hollow leaves.
    2.  Cercospora leaf spot disease: causes significant losses, especially in late summer (high temperature, high humidity, long leaf wet periods throughout the night). Impact: beets fail to grow to full size if severe. Controlled by spraying Mencozeb 2 g/L.
    3.  Rhizoctonia Root Rot. Impact: kills and stunts plants. Controlled with Carbendazim 1 g/L (GreenMyLife, 2018).
     
    The nutritional composition of beets in 100 grams of ingredients as stated in the 2017 Indonesian Food Comp-osition Table (TKPI) and 2018 United States Department  of Agriculture (USDA) can be seen in the Table 1.

    Table 1: Composition of nutrients in 100 g of beets.


         
    Beets not only consist of macronutrients and micronutrients, but beets are a functional food source because they have benefits for various diseases by containing important components called bioactive compounds such as vitamins, minerals, phenols, carotenoids, nitrates, ascorbic acid and betalains. The effects of phytochemicals depend on the bioaccessibility of nutrients during the digestive process (Liliana and Oana-Viorela, 2020).
           
    Beets are also a plant that is rich in nitrates, so beets are a plant that is high in nitrate content. Table 2 shows the average nitrate content in vegetables in mg/kg, mmol in UK portions as a guide to estimating the number of nitrate units per portion (1 nitrate unit = 1 mmol) to estimate nitrate intake or to modify/alter intake as desired. Tap water and mineral water are included in the table intended for comparison (Lidder and Webb, 2013).

    Table 2: Nitrate content in plants (Lidder dan Webb 2013).


           
    Beetroot are an important source of inorganic nitrate with varying amounts of nitrate. It is reported that there is a 10-fold variation between single varieties (Mirmiran, 2020). Some studies report nitrate levels in beetroot ranging from 644 - 1800 mg/kg (Lidder and Webb, 2013), although some studies found higher amounts of nitrate in beetroot, such as beetroot juice containing 4965 mg/L nitrate (Corleto et al., 2018). Raw beetroot contains 4420 mg/kg but this amount increases drastically to 42415 mg/kg after the dehydration process (Sucu and Turp, 2018), likewise, beetroot powder contains 14037 mg/kg nitrate (Ozaki et al., 2021). In addition, fermenting beetroot juice and extract allows the conversion of nitrates to nitrites first (Choi et al., 2017), thus increasing the protective effect, which can be added to meat products in the form of nitrites (Hwang et al., 2017; 2018).
     
    Nitrate and nitrite production in plants
     
    Nitrate  and  nitrite  is  produced  in  plant  by  nitrogen  cycle.  Nitrogen  cycle  is  a fundamental biogeochemical process of a crop development that converts nitrogen into various forms,  allowing  it  to  move  from  the  atmosphere  to  the  soil,  organisms,  and  back  to  the atmosphere (Astier; 2018; Valenzuela, 2023). Atmospheric N becomes available to plants via a series of microbial transformations in the soil (Geisseler, 2010; Grzyb, 2021). The process of the  nitrogen  cycle  consists  of  several  stages,  including  nitrogen  fixation, nitrification, assimilation, ammonification and  denitrifi-cation  (Grzyb, 2021; Brochado et al., 2023).  Nitrogen fixation is the initial step of the nitrogen cycle, where atmospheric nitrogen (N2) is converted into ammonia (NH3).The symbiotic nitrogen fixation is an indispensable process in the nitrogen cycle, where bacteria of the genus Rhizobium establish symbiotic associations with leguminous plants, such as the common bean (Phaseolus vulgaris), soybean (Glycine max) and pea (Pisum sativum) (Brito, 2011; Cunha, 2023; Kamran, 2023). These bacteria have the ability to convert atmospheric nitrogen into a form assimilable by plants (Brochado et al., 2023).
           
    After nitrogen fixation, the next stages is nitrification which converting ammonia (NH3) into nitrite (NO2) and then into nitrate (NO3). This process is carried out by nitrifying bacteria in the soil, ammonia (NH3) is first converted into nitrite by Nitrosomonas bacteria and then into nitrate by Nitrobacter bacteria. Nitrates (NO3) are the primary source of nitrogen for plants and they  can  be  taken  up  by  plant  roots and used  to  synthesize  amino  acids  and other nitrogen- containing compounds (Valenzuela, 2023). Nitrification plays a crucial role in transforming organic nitrogen compounds into readily accessible inorganic forms for plants  (Brochado, 2023).
           
    Assimilation is a next stages that incorporating ammonia (NH3) and nitrates (NO3-) into biological tissues, such as plant and animal cells. This incorporation allows organisms to utilize nitrogen for the synthesis of essential molecules, such as proteins and nucleic acids (Mokhele, 2012,  Zhu, 2023).  After  assimilation,  processing  of  ammonification  occur  when  organisms excrete  waste  or  die, the  nitrogen  in  their  tissues  is  in  the  form  of  organic  nitrogen.  Various fungi and prokaryotes then decompose the tissue and release inorganic nitrogen back into the environment,  making it available for uptake by plants and other  microorganisms for growth (Kuypers, 2018). Nitrate-N that is not taken up by plants, because it is soluble, may be leached below  the root  zone, it may be converted to  dinitrogen (N2) or nitrous  oxide  (N2O)  gases  by heterotrophic bacteria, called denitrification process (Grzyb, 2021; Wang, 2022).
     
    Red beetroot as a functional food
     
    Benefits of red beetroot as a functional ingredient in various food products
     
    Beetroots can have added value if they can be made into a product (Table 3). Beetroot can be formulated as fresh juice, fermented juice, bread, powder, chips, gel and cereal-bar which have been tested on healthy and unhealthy volunteers as a food supplement. Several products made from red beetroot are in great demand among the public, such as juice, yogurt, candy, jam, jelly, powder and ice cream (Czyżewska et al., 2006; Baião et al., 2017; 2018; Hobbs et al., 2014). Red beetroot is a tuber vegetable rich in nutrients and bioactive compounds, traditionally used in various food products because of its red color. Cereal-based products such as bread, pastries, biscuits, pasta and noodles are food sources of carbohydrates and protein but lack micronutrients and fiber, thereby increasing consumer demand for healthy foods that provide nutrient-dense foods (Rousta et al., 2021).

    Table 3: Application of red beetroot in food products (Sneh et al. 2022).


           
    The addition of red beetroot fiber to bread, rolls, cakes, cupcakes, biscuits and cookies can increase the fiber, ash and protein content while reducing the fat content due to the higher nutritional content of beetroot powder (Hobbs et al., 2014; Nagib and Zidan 2019;  Daunaravičiūtė et al., 2020). Beetroots can be added to ready-to-eat snacks such as extruded products and breakfast cereals. Formulated as a functional snack with an attractive pink to red color it is very popular with consumers because of its delicious taste, texture and attractive appearance (Abdul Alam et al., 2018; Lisiecka and Wójtowicz, 2021). Red beetroot powder and beetroot juice can be used as a natural coloring in butter, mayonnaise, cream cheese spread and cream cheese which functions as a natural antimicrobial, reduces lipid oxides, suppresses the growth of bacteria and fungi and reduces peroxide levels. This is because the antioxidant activity of beetroots is higher, resulting in dairy products with a longer shelf life (Raikos et al., 2016, Asadaii et al., 2020).
           
    The addition of beetroots in milk-based drinks such as yogurt and fermented buttermilk drinks can reduce acidity, increase antioxidant properties, antibacterial potential, total phenolic content, survival of probiotic bacteria Streptococcus thermophiles and Lactobacillus and increase consumer acceptance (Ganguly et al., 2017; Hashem 2018; Ahmad and Ali, 2019). The addition of 10% red beetroot powder to cookies is more acceptable (Murlidhar et al., 2017) and the quality of spray-dried beetroot powder stored for a long period is better stored in LAP packaging compared to HDPE (Singh and Hathan, 2017). The addition of 10% beetroot powder can also increase the elasticity of snack bars, significantly reduce hardness, the most acceptable texture and sensory properties, have higher ash content, carbohydrates, antioxidant activity, flavonoids and total phenols (Tangariya et al., 2022). Consumption of functional beetroot gelly is a new strategy to provide nutritional content with high bioaccessibility such as nitrate, potassium and antioxidants which have the potential to improve heart health and sports performance (Silva et al., 2016; Morgado et al., 2016).
     
    Health benefits of nitrate and nitrite in red beetroot
     
    Nitrates (NO3-)  and  nitrites  (NO2-)  are  naturally  occurring  substances  in  fruits  and   vegetables, which humans are encouraged to consume because of their beneficial health effects. On the other side, nitrates and nitrites are used as food additives such as sausages, ham and other processed meat (Levine, 2012; Song, 2015). Nitrate and nitrite in humans are present due to diet or produced by the action of endogenous L-arginine-NO synthase (Nuji, 2017; Mcneal, 2021). Nitrate (NO3-) in food is converted in the human body to nitrite (NO2-) and subsequently to nitric oxide (NO) generated by NOS (NO synthase) enzymes that oxidize in the blood and tissue. In the blood, exogenous NO3 mixes with endogenous NO3- produced via the oxidation of NO (Shannon, 2021; Redaelli, 2022).
           
    Nitric oxide in the body is a compound that is known to have beneficial effects for clinical application. NO could regulate metabolic disorder-induced cardiovascular diseases and other metabolic disease, such as reduced blood pressure and increased oxygen and nutrient delivery to the active muscle and also as a mediator for neurotrans-mission, vasodilatation, nerve function and immune defense (Ma, 2018; Zamani, 2021; Andrabi, 2023). Under conditions of illness or senescence, the activity of eNOS (endothelial nitric oxide synthase) was reduced  and  the production of NO was decreased  (Novensa, 2011; Rogers, 2013). Thus indicating exogenous source of NO supplement might have a potential treatment for patients undergoing illness or senescence (Ma, 2018).
           
    NO is known to be a potent vasodilator to cause a BP reduction. NO generated in the vasculature causes  relaxation in vascular smooth  muscle,  which  subsequently  results in vasodilation (Levine, 2012; Redaelli, 2022). The nitrite anion is a cell-signaling molecule, which is considered a storage pool of NO as well as a NO-independent signal. Dietary nitrate- enhanced nitrite is capable of increasing cyclic guanosine 32 ,52 -monophosphate (cGMP) levels in tissues and contributing to blood vessel vasodilation via a mechanism that lies upstream from activation of soluble guanylyl cyclase (sGC) (Liu, 2020).
           
    Moreover, the synthesis of NO was reduced in obese mice (Siervo, 2011). Metabolic disorder-induced high blood pressure, insulin resistance and carbohydrate tolerance were found in eNOS (endothelial nitric oxide synthase)-knockout mice. Dietary nitrate effectively supplements NO by the activated exogenous NO3-NO2-NO pathway under conditions of hypoxia. Nitrate enhanced exercise tolerance by the NO-cGMP-PPAR pathway and increased the metabolism of fatty acid in skeletal muscle cells (Ashmore, 2015). Exogenous nitrate could activate the cGMP pathway in mice and promote the conversion of white adipose to brown adipose, therefore enhancing fat metabolism and decreasing body weight (Roberts, 2015).
                   
    NO also contributes to improved wound healing by upregulating angiogenic factors, such as TGF-ß and VEGF, which ensures adequate blood supply for healing. However, in cases of impaired wound healing, inadequate NO synthases and low levels of available NO lead to decreased collagen deposition, unregulated inflammatory responses, tissue hypoxia and prolonged healing time (Malone-Povolny, 2019). Recently, hypoxia-induced oxidative stress conditions have been suggested to facilitate the depletion of antioxidants and thus promote cysteine oxidation and subsequently lead to an enhanced Cgb generation of NO in the presence of nitrite during hypoxia (Bescós, 2012; Reeder, 2018).

    CONCLUSION

    Red beetroot is a superfood that has been used as a therapeutic and functional food ingredient since ancient times. This paper summarizes the entire scope of red beetroot and its use as a value-added product. It is useful as a food coloring agent in many dairy and food products. The Nitrate content in red beets through the physiological role of NO which functions as vasodilation, efficient use of O2 during exercise, the immune system, as a neurotransmitter and as an inhibitor of platelet adhesion. It also has anti-microbial, anti-hypertensive, anti- inflammatory, anti-hyperglycemic properties, etc. This plant has many health benefits and provides an opportunity for researchers to develop various products derived from red beets that have added value.

    ACKNOWLEDGEMENT

    The present study was supported by Brawijaya University and the Ministry of Health of the Republic of Indonesia through the Malang Ministry of Health Health Polytechnic.
     
    Disclaimers
     
    The views and conclusions expressed in this article are solely those of the authors and do not necessarily represent the views of their affiliated institutions. The authors are responsible for the accuracy and completeness of the information provided, but do not accept any liability for any direct or indirect losses resulting from the use of this content.

    Informed consent
     
    All animal procedures for experiments were approved by the Committee of Experimental Animal care and handling techniques were approved by the University of Animal Care Committee.

    CONFLICT OF INTEREST

    The authors declare that there are no conflicts of interest regarding the publication of this article. No funding or sponsorship influenced the design of the study, data collection, analysis, decision to publish, or preparation of the manuscript.

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